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Equiluminance Cells in Visual Cortical Area V4

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Equiluminance Cells in Visual Cortical Area V4 12398 • The Journal of Neuroscience, August 31, 2011 • 31(35):12398–12412 Behavioral/Systems/Cognitive Equiluminance Cells in Visual Cortical Area V4 Brittany N. Bushnell,1 Philip J. Harding,1 Yoshito Kosai,1 Wyeth Bair,1,2 and Anitha Pasupathy1 1Department of Biological Structure and Washington National Primate Research Center, University of Washington, Seattle, Washington 98195, and 2Department of Physiology, Anatomy, and Genetics, University of Oxford, Oxford OX1 3PT, United Kingdom We report a novel class of V4 neuron in the macaque monkey that responds selectively to equiluminant colored form. These “equilumi- nance” cells stand apart because they violate the well established trend throughout the visual system that responses are minimal at low luminance contrast and grow and saturate as contrast increases. Equiluminance cells, which compose ϳ22% of V4, exhibit the opposite behavior: responses are greatest near zero contrast and decrease as contrast increases. While equiluminance cells respond preferentially to equiluminant colored stimuli, strong hue tuning is not their distinguishing feature—some equiluminance cells do exhibit strong unimodal hue tuning, but many show little or no tuning for hue. We find that equiluminance cells are color and shape selective to a degree comparable with other classes of V4 cells with more conventional contrast response functions. Those more conventional cells respond equally well to achromatic luminance and equiluminant color stimuli, analogous to color luminance cells described in V1. The existence of equiluminance cells, which have not been reported in V1 or V2, suggests that chromatically defined boundaries and shapes are given special status in V4 and raises the possibility that form at equiluminance and form at higher contrasts are processed in separate channels in V4. Introduction nance contrast on chromatic responses is typically facilitatory. Responses of neurons in primate area V4, an intermediate Most neurons in V1, V2, and V3 are sensitive to both luminance stage along the ventral visual pathway, are sensitive to the and color (Gouras and Kruger, 1979; Thorell et al., 1984; Hubel color (Zeki, 1973; Schein and Desimone, 1990) and the ach- and Livingstone, 1990; Lennie et al., 1990; Johnson et al., 2001; romatic luminance of visual stimuli (Schein and Desimone, Hansen and Gegenfurtner, 2007), and the contrast response 1990). But, because studies seldom vary chromaticity and lu- functions in these areas show a characteristic V-shaped pattern minance simultaneously, we do not yet know how luminance (i.e., responses increase, and saturate, with increasing luminance and chromatic signals are multiplexed in area V4. This is an contrasts) (Sclar et al., 1990; Albrecht, 1995; Gegenfurtner et al., important question to address because (1) V4 is known to play an 1997; Kiper et al., 1997). A small fraction of V1 neurons respond important role in form processing (Desimone and Schein, 1987; more strongly to equiluminant stimuli than to luminance stim- Kobatake and Tanaka, 1994); (2) in natural vision, form can be uli, but because these neurons are typically low pass and unori- defined by chromatic contrast, luminance contrast, or both ented (Lennie et al., 1990; Johnson et al., 2001), they are unlikely (Hansen and Gegenfurtner, 2009); and (3) psychophysical stud- to contribute to form encoding. The V1 and V2 neurons ies suggest that both chromatic and luminance contrasts contrib- equipped to encode object boundaries multiplex luminance and ute to form perception (Cavanagh, 1991). Deciphering how color signals (Lennie et al., 1990; Johnson et al., 2001; Shapley and luminance and chrominance signals are combined across the V4 Hawken, 2002; Hansen and Gegenfurtner, 2007). population will advance our understanding of how cortex pro- To discover how luminance contrast modulates the responses duces a unified, invariant perception of form. of V4 neurons to colored stimuli, we studied the responses of Evidence from early stages of visual processing suggests that single neurons in awake monkeys to a set of 25 chromaticities chrominance-defined and luminance-defined form information presented at four different luminance contrasts. As in V1, a ma- is carried by the same neurons and that the influence of lumi- jority of V4 neurons responded to both chromatic and achro- matic stimuli, and luminance contrast had a facilitatory influence on chromatic responses. For a sizable minority, however, equilu- Received April 14, 2011; revised June 25, 2011; accepted July 8, 2011. minant color stimuli evoked the strongest responses, which de- Author contributions: P.J.H., W.B., and A.P. designed research; B.N.B., P.J.H., Y.K., and A.P. performed research; creased when luminance contrasts were added to the chromatic A.P. analyzed data; W.B. and A.P. wrote the paper. stimuli. These equiluminance cells do not fall into previously This work was supported by National Eye Institute Grant R01 EY018839, The Whitehall Foundation, University of Washington Vision Core Grant P30 EY01730, and National Center for Research Resources Grant RR00166. W.B. is established cell classes in V1 or V2, and their shape-selective supportedbytheWellcomeTrustandSt.John’sCollege,Oxford(Oxford,UK).WethankYasmineEl-Shamayleh,Greg properties suggest that these neurons can contribute to the en- Horwitz, and Raghu Pasupathy for helpful discussions and comments. Jalal Baruni and National Primate Research coding of equiluminant colored form. Center Bioengineering provided technical support. Correspondence should be addressed to Anitha Pasupathy, Department of Biological Structure and Washington NationalPrimateResearchCenter,UniversityofWashington,1959PacificStreetNortheast,HSBG-520,Universityof Materials and Methods Washington Mailbox 357420, Seattle, WA 98195. E-mail: [email protected]. Surgery and animal behavior DOI:10.1523/JNEUROSCI.1890-11.2011 Two rhesus monkeys (Macaca mulatta; one male and one female) were Copyright © 2011 the authors 0270-6474/11/3112398-15$15.00/0 surgically implanted with custom-built head posts attached to the skull Bushnell et al. • Equiluminance Cells in V4 J. Neurosci., August 31, 2011 • 31(35):12398–12412 • 12399 with orthopedic screws. After fixation training (see below), a recording chamber was implanted based on structural MRI scans. A craniotomy was performed in a subsequent surgery. For detailed surgical procedures, see Bushnell et al. (2011). All animal procedures conformed to NIH guidelines and were approved by the Institutional Animal Care and Use Committee at the University of Washington. Animals were seated in front of a computer monitor at a distance of 57 cm and were trained to fixate a 0.1° white dot within 0.5–0.75° of visual angle. Eye position was monitored using a 1 kHz infrared eye-tracking system (Eyelink 1000; SR Research). Stimulus presentation and animal behavior were controlled by Linux-based custom software (PYPE; orig- inally developed in the Gallant Laboratory, University of California, Berkeley, Berkeley, CA). Each trial began with the presentation of a fix- ation spot at the center of the screen. Once fixation was acquired, four to six stimuli were presented in succession, each for 300 ms (500 ms for 22 cells), separated by interstimulus intervals of 200 ms. Stimulus onset and offset times were based on photodiode detection of synchronized pulses in the lower left corner of the monitor. Data collection During each recording session, a single dura-puncturing microelectrode (FHC), 250 ␮m in diameter, was lowered into the cortex using an eight- channel acute microdrive system (Gray Matter Research). Signals from the electrode were amplified and filtered and single-neuron activity was isolated using a spike sorting system (Plexon Systems). We targeted dorsal V4 and our electrode penetrations were largely in the prelunate gyrus and occasionally in the adjoining bank of the lunate Figure1. Colorandshapestimuli.A,The25chromaticitiesusedinthestudyareshownintheCIE sulcus. Previous studies suggest that color selective units are clustered in chromaticitydiagram.Thecolorsoccupiedthreetrianglesatincreasingdistancesfromtheachromatic patches, recently termed “globs” (Conway et al., 2007). While the precise point(no.1)andrepresentedthreelevelsofcolorcontrast:colors2–7composedthelowcolorcontrast location of globs varies across animals, combining fMRI and physiology, band; 8–13, the mid color contrast band; and 14–25, the high color contrast band. Each of the 25 Conway and colleagues suggested that globs were less prevalent in dorsal chromaticities was presented at four different luminance contrasts relative to the achromatic V4. We do not know the precise location of globs in our animals, but background labeled 1. B, Shape stimuli used to characterize the shape preferences of neurons. 15–20% of our recorded neurons had hue tuning (see Results) that was A subset (10–29) of these shapes was presented in eight orientations at 45° intervals to study roughly consistent with that attributed to glob regions. shape selectivity. Some shapes that show rotational symmetry were presented at fewer rota- tions. For example, shapes labeled 1 and 2 were presented at two and four rotations, respec- Visual stimuli tively. Shape labeled 1 was used to characterize color and luminance preferences of example Visual stimuli were presented on a CRT monitor (40.6 ϫ 30.5 cm; 97 Hz ϫ neuronswhosedataareshowninFigure2,A,B,andD;shapelabeled2wasusedtocharacterize frame rate; 1600 1200 pixels) calibrated with a spectrophotoradiom-
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